Peripheral changes in endometriosis-associated pain

Human Reproduction Update

Volumn 20, Issue 5, 2014, Pages 717-736

  Morotti, Matteo ^a,b   Vincent, Katy ^a   Brawn, Jennifer ^a   Zondervan, Krina T ^a,c   Becker, Christian M ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Endometriosis; Nerve fibres; Neuroangiogenesis; Neurotrophins; Peripheral changes

Indexed keywords

NEUROTROPHIC FACTOR; NEUROTROPHIN;

CINAHL; EMBASE; ENDOMETRIOSIS; ENDOMETRIUM TUMOR; HUMAN; MEDLINE; NERVE FIBER; PAIN; PATHOPHYSIOLOGY; PELVIC PAIN; PERIPHERAL NERVOUS SYSTEM; PERITONEAL FLUID; PRIORITY JOURNAL; REVIEW; SYSTEMATIC REVIEW; UPREGULATION;

ENDOMETRIOSIS; NERVE FIBRES; NEUROANGIOGENESIS; NEUROTROPHINS; PERIPHERAL CHANGES;

ASCITIC FLUID; ENDOMETRIOSIS; ENDOMETRIUM; FEMALE; HUMANS; NEOVASCULARIZATION, PATHOLOGIC; NERVE FIBERS; NEUROGENESIS; PAIN;

EID: 84906066845     PISSN: 13554786     EISSN: 14602369     Source Type: Journal    
DOI: 10.1093/humupd/dmu021     Document Type: Review

References (205)

1. Adams RH, Eichmann A. Axon guidance molecules in vascular patterning. Cold Spring Harb Perspect Biol 2010;2:a001875.
2. Aghaey Meibody F, Mehdizadeh Kashi A, Zare Mirzaie A, Ghajarie Bani Amam M, Shariati Behbahani A, Zolali B, Najafi L. Diagnosis of endometrial nerve fibers in women with endometriosis. Arch Gynecol Obstet 2011;284:1157-1162.
3. Agic A, von Wussow U, Starzinski-Powitz A, Diedrich K, Altevogt P, Hornung D. Inhibition of cell proliferation, adhesion, and invasion with an anti-L1-cell adhesion molecule monoclonal antibody in an in vitro endometriosis model. Fertil Steril 2010;94:1102-1104.
4. Al-Fozan H, Bakare S, Chen MF, Tulandi T. Nerve fibers in ovarian dermoid cysts and endometriomas. Fertil Steril 2004;82:230-231.
5. Al-Jefout M, Andreadis N, Tokushige N, Markham R, Fraser I. A pilot study to evaluate the relative efficacy of endometrial biopsy and full curettage in making a diagnosis of endometriosis by the detection of endometrial nerve fibers. Am J Obstet Gynecol 2007;197:578.e1-4.
6. Al-Jefout M, Dezarnaulds G, Cooper M, Tokushige N, Luscombe GM, Markham R, Fraser IS. Diagnosis of endometriosis by detection of nerve fibres in an endometrial biopsy: a double blind study. Hum Reprod 2009;24:3019-3024.
7. Anaf V, Simon P, El Nakadi I, Fayt I, Buxant F, Simonart T, Peny MO, Noel JC. Relationship between endometriotic foci and nerves in rectovaginal endometriotic nodules. Hum Reprod 2000;15:1744-1750.
8. Anaf V, Simon P, El Nakadi I, Fayt I, Simonart T, Buxant F, Noel JC. Hyperalgesia, nerve infiltration and nerve growth factor expression in deep adenomyotic nodules, peritoneal and ovarian endometriosis. Hum Reprod 2002;17:1895-1900.
9. Anaf V, El Nakadi I, Simon P, Van de Stadt J, Fayt I, Simonart T, Noel JC. Preferential infiltration of large bowel endometriosis along the nerves of the colon. Hum Reprod 2004;19:996-1002.
10. Anaf V, Chapron C, El Nakadi I, De Moor V, Simonart T, Noël JC. Pain, mast cells, and nerves in peritoneal, ovarian, and deep infiltrating endometriosis. Fertil Steril 2006; 86:1336-1343.
11. Arese M, Serini G, Bussolino F. Nervous vascular parallels: axon guidance and beyond. Int J Dev Biol 2011;55:439-445.
12. Arnold J, Barcena de Arellano ML, Rüster C, Vercellino GF, Chiantera V, Schneider A, Mechsner S. Imbalance between sympathetic and sensory innervation in peritoneal endometriosis. Brain Behav Immun 2012;26:132-141.
13. Arnold J, Vercellino GF, Chiantera V, Schneider A, Mechsner S, Barcena de Arellano ML. Neuroimmunomodulatory alterations in non-lesional peritoneum close to peritoneal endometriosis. Neuroimmunomodulation 2013;20:9-18.
14. Asami T, Ito T, Fukumitsu H, Nomoto H, Furukawa Y, Furukawa S. Autocrine activation of cultured macrophages by brain-derived neurotrophic factor. Biochem Biophys Res Commun 2006;344:941-947.
15. Asante A, Taylor RN. Endometriosis: the role of neuroangiogenesis. Annu Rev Physiol 2011;73:163-182.
16. As-Sanie S, Harris RE, Napadow V, Kim J, Neshewat G, Kairys A, Williams D, Clauw DJ, Schmidt-Wilcke T. Changes in regional gray matter volume in women with chronic pelvic pain: a voxel-based morphometry study. Pain 2012;153:1006-1014.
17. Atwal JK, Singh KK, Tessier-Lavigne M, Miller FD, Kaplan DR. Semaphorin 3F antagonizes neurotrophin-induced phosphatidylinositol 3-kinase and mitogenactivated protein kinase kinase signaling: a mechanism for growth cone collapse. J Neurosci 2003;23:7602-7609.
18. Atwal G, du Plessis D, Armstrong G, Slade R, Quinn M. Uterine innervation after hysterectomy for chronic pelvic pain with, and without, endometriosis. Am J Obstet Gynecol 2005;193:1650-1655.
19. Bandtlow CE, Meyer M, Lindholm D, Spranger M, Heumann R, Thoenen H. Regional and cellular codistribution of interleukin 1 beta and nerve growth factor mRNA in the adult rat brain: possible relationship to the regulation of nerve growth factor synthesis. J Cell Biol 1990;111:1701-1711.
20. Barcena de Arellano ML, Arnold J, Vercellino F, Chiantera V, Schneider A, Mechsner S. Overexpression of nerve growth factor in peritoneal fluid from women with endometriosis may promote neurite outgrowth in endometriotic lesions. Fertil Steril 2011a;95:1123-1126.
21. Barcena de Arellano ML, Arnold J, Vercellino GF, Chiantera V, Ebert AD, Schneider A, Mechsner S. Influence of nerve growth factor in endometriosis-associated symptoms. Reprod Sci 2011b;18:1202-1210.
22. Barcena de Arellano ML, Arnold J, Sacher F, Blochle M, Staube M, Bartley J, Vercellino GF, Chiantera V, Schneider A, Mechsner S. Eutopic endometrium from women with endometriosis does not exhibit neurotrophic properties. J Neuroimmunol 2012a;249:49-55.
23. Barcena de Arellano ML, Wagner MF, Oldeweme J, Arnold J, Ebert A, Schneider A, Mechsner S. Neurotrophin expression is not affected in uteri of women with adenomyosis. J Mol Neurosci 2012b;47:495-504.
24. Barcena de Arellano ML, Arnold J, Lang H, Vercellino GF, Chiantera V, Schneider A, Mechsner S. Evidence of neurotrophic events due to peritoneal endometriotic lesions. Cytokine 2013a;62:253-261.
25. Barcena de Arellano ML, Münch S, Arnold J, Helbig S, Schneider A, Mechsner S. Calcium-binding protein expression in peritoneal endometriosis-associated nerve fibres. Eur J Pain 2013b;17:1425-1437.
26. Barcena de Arellano ML, Oldeweme J, Arnold J, Schneider A, Mechsner S. Remodeling of estrogen-dependent sympathetic nerve fibers seems to be disturbed in adenomyosis. Fertil Steril 2013c;100:801-809.
27. Becker CM, D'Amato RJ. Angiogenesis and antiangiogenic therapy in endometriosis. Microvasc Res 2007;74:121-130.
28. BeckerCM, Sampson DA, Rupnick MA, Rohan RM, Efstathiou JA, Short SM, Taylor GA, Folkman J, D'Amato RJ. Endostatin inhibits the growth of endometriotic lesions but does not affect fertility. Fertil Steril 2005;84:1144-1155.
29. Becker CM, Beaudry P, Funakoshi T, Benny O, Zaslavsky A, Zurakowski D, Folkman J, D'Amato RJ, Ryeom S. Circulating endothelial progenitor cells are up-regulated in a mouse model of endometriosis. Am J Pathol 2011;178:1782-1791.
30. Bergqvist A, Bruse C, Carlberg M, Carlström K. Interleukin 1beta, interleukin-6, and tumor necrosis factor-alpha in endometriotic tissue and in endometrium. Fertil Steril 2001;75:489-495.
31. Berkley KJ, Dmitrieva N, Curtis KS, Papka RE. Innervation of ectopic endometrium in a rat model of endometriosis. Proc Natl Acad Sci USA 2004;101:11094-11098.
32. Berkley KJ, Rapkin AJ, Papka RE. The pains of endometriosis. Science 2005;308: 1587-1589.
33. Berkley KJ, McAllister SL, Accius BE, Winnard KP. Endometriosis-induced vaginal hyperalgesia in the rat: effect of estropause, ovariectomy, and estradiol replacement. Pain 2007;132:S150-S159.
34. Bjorling DE, Beckman M, Clayton MK,Wang ZY. Modulation of nerve growth factor in peripheral organs by estrogen and progesterone. Neuroscience 2002;110:155-167.
35. Boissé L, Chisholm SP, Lukewich MK, Lomax AE. Clinical and experimental evidence of sympathetic neural dysfunction during inflammatory bowel disease. Clin Exp Pharmacol Physiol 2009;36:1026-1033.
36. Bokor A, Kyama CM, Vercruysse L, Fassbender A, Gevaert O, Vodolazkaia A, De Moor B, Fülöp V, D'Hooghe T. Density of small diameter sensory nerve fibres in endometrium: a semi-invasive diagnostic test for minimal to mild endometriosis. Hum Reprod 2009;24:3025-3032.
37. Brawn J, Morotti M, Zondervan KT, Becker CM, Vincent K. Central changes associated with chronic pelvic pain and endometriosis. Human reproduction update 2014; 20:737-747.
38. Browne AS, Yu J, Huang RP, Francisco AM, Sidell N, Taylor RN. Proteomic identification of neurotrophins in the eutopic endometrium of women with endometriosis. Fertil Steril 2012;98:713-719.
39. Bulun SE. Endometriosis. N Engl J Med 2009;360:268-279.
40. Bulun SE, Monsavais D, Pavone ME, Dyson M, Xue Q, Attar E, Tokunaga H, Su EJ. Role of estrogen receptor-β in endometriosis. Semin Reprod Med 2012;30:39-45.
41. Burney RO, Giudice LC. Pathogenesis and pathophysiology of endometriosis. Fertil Steril 2012;98:511-519.
42. Butterworth JF IV, Strichartz GR. Molecular mechanisms of local anesthesia: a review. Anesthesiology 1990;72:711-734.
43. Cantarella G, Lempereur L, Presta M, Ribatti D, Lombardo G, Lazarovici P, Zappalà G, Pafumi C, Bernardini R. Nerve growth factor-endothelial cell interaction leads to angiogenesis in vitro and in vivo. FASEB J 2002;16:1307-1309.
44. Capobianco A, Rovere-Querini P. Endometriosis, a disease of the macrophage. Front Immunol 2013;4:9.
45. Carmeliet P, Tessier-Lavigne M. Common mechanisms of nerve and blood vessel wiring. Nature 2005;436:193-200.
46. Cason AM, Samuelsen CL, Berkley KJ. Estrous changes in vaginal nociception in a rat model of endometriosis. Horm Behav 2003;44:123-131.
47. Chapron C, Fauconnier A, Dubuisson JB, Barakat H, Vieira M, Breárt G. Deep infiltrating endometriosis: relation between severity of dysmenorrhoea and extent of disease. Hum Reprod 2003;18:760-766.
48. Chen Y, Michaelis M, Janig W, Devor M. Adrenoreceptor subtype mediating sympathetic-sensory coupling in injured sensory neurons. J Neurophysiol 1996; 76:3721-3730.
49. Chen Y, Li D, Zhang Z, Takushige N, Kong BH, Wang GY. Effect of siRNA Against b-NGF on Nerve Fibers of a Rat Model With Endometriosis. Reprod Sci 2014; 21:329-339.
50. Choi YS, Cho S, Lim KJ, Jeon YE, Yang HI, Lee KE, Heena K, Seo SK, Kim HY, Lee BS. Effects of LNG-IUS on nerve growth factor and its receptors expression in patients with adenomyosis. Growth Factors 2010;28:452-460.
51. Coosemans A, Moerman P, Vergote I, Koninckx PR, Van Gool SW, Amant F. Wilms' tumor gene 1 (WT1) overexpression in neurons in deep endometriosis: a pilot study. Fertil Steril 2009;91:1441-1444.
52. Cornillie FJ, Oosterlynck D, Lauweryns JM, Koninckx PR. Deeply infiltrating pelvic endometriosis: histology and clinical significance. Fertil Steril 1990;53: 978-983.
53. Craft RM. Modulation of pain by estrogens. Pain 2007;132:S3-12.
54. Daniels JP, Middleton L, Xiong T, Champaneria R, Johnson NP, Lichten EM, Sutton C, Vercellini P, Gray R, Hills RK et al. International LUNA IPD Meta-analysis Collaborative Group. Individual patient data meta-analysis of randomized evidence to assess the effectiveness of laparoscopic uterosacral nerve ablation in chronic pelvic pain. Hum Reprod Update 2010;16:568-576.
55. Dawson NJ, Schmid H, Pierau FK. Pre-spinal convergence between thoracic and visceral nerves of the rat. Neurosci Lett 1992;138:149-152.
56. D'Hooghe TM, Mihalyi AM, Simsa P, Kyama CK, Peeraer K, De Loecker P, Meeuwis L, Segal L, Meuleman C.Why we need a noninvasive diagnostic test for minimal to mild endometriosis with a high sensitivity. Gynecol Obstet Invest 2006;62:136-138.
57. Dickson BJ. Molecular mechanisms of axon guidance. Science 2002;298:1959-1964.
58. Dunselman GA, Vermeulen N, Becker C, Calhaz-Jorge C, D'Hooghe T, De Bie B, Heikinheimo O, Horne AW, Kiesel L, Nap A et al. ESHRE guideline: management of women with endometriosis. Hum Reprod 2014;29:400-412.
59. Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol 1995;146:1029-1039.
60. Eichmann A, Makinen T, Alitalo K. Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev 2005;19:1013-1021.
61. Emanueli C, Salis MB, Pinna A, Graiani G, Manni L, Madeddu P. Nerve growth factor promotes angiogenesis and arteriogenesis in ischemic hindlimbs. Circulation 2002; 106:2257-2262.
62. Erskine L, Reijntjes S, Pratt T, Denti L, Schwarz Q, Vieira JM, Alakakone B, Shewan D, Ruhrberg C. VEGF signaling through neuropilin 1 guides commissural axon crossing at the optic chiasm. Neuron 2011;70:951-965.
63. Eskandari F,Webster JI, Sternberg EM. Neural immune pathways and their connection to inflammatory diseases. Arthritis Res Ther 2003;5:251-265.
64. Eskenazi B,Warner ML. Epidemiology of endometriosis. Obstet Gynecol Clin North Am 1997;24:235-258.
65. Fassbender A, Vodolazkaia A, Saunders P, Lebovic D, Waelkens E, De Moor B, D'Hooghe T. Biomarkers of endometriosis. Fertil Steril 2013;99:1135-1145.
66. Fassold A, FalkW, Anders S, Hirsch T, Mirsky VM, Straub RH. Soluble neuropilin-2, a nerve repellent receptor, is increased in rheumatoid arthritis synovium and aggravates sympathetic fiber repulsion and arthritis. Arthritis Rheum 2009; 60:2892-2901.
67. Fauconnier A, Chapron C. Endometriosis and pelvic pain: epidemiological evidence of the relationship and implications. Hum Reprod Update 2005;11:595-606.
68. Fauconnier A, Chapron C, Dubuisson JB, Vieira M, Dousset B, Breárt G. Relation between pain symptoms and the anatomic location of deep infiltrating endometriosis. Fertil Steril 2002;78:719-726.
69. Fernandes ES, Fernandes MA, Keeble JE. The functions of TRPA1 and TRPV1: moving away from sensory nerves. Br J Pharmacol 2012;166:510-521.
70. Ferrero S, Haas S, Remorgida V, Camerini G, Fulcheri E, Ragni N, Straub RH, Capellino S. Loss of sympathetic nerve fibers in intestinal endometriosis. Fertil Steril 2010;94:2817-2819.
71. Fuh G, Garcia KC, de Vos AM. The interaction of neuropilin-1 with vascular endothelial growth factor and its receptor flt-1. J Biol Chem 2000;275:26690-26695.
72. Gelfand MV, Hong S, Gu C. Guidance from above: common cues direct distinct signaling outcomes in vascular and neural patterning. Trends Cell Biol 2009; 19:99-110.
73. Geretti E, Shimizu A, Klagsbrun M. Neuropilin structure governs VEGF and semaphorin binding and regulates angiogenesis. Angiogenesis 2008;11:31-39.
74. Giamberardino MA, De Laurentis S, Affaitati G, Lerza R, Lapenna D, Vecchiet L. Modulation of pain and hyperalgesia from the urinary tract by algogenic conditions of the reproductive organs in women. Neurosci Lett 2001;304:61-64.
75. Giamberardino MA, Costantini R, Affaitati G, Fabrizio A, Lapenna D, Tafuri E, Mezzetti A. Viscero-visceral hyperalgesia: characterization in different clinical models. Pain 2010;151:307-322.
76. Giudice LC, Kao LC. Endometriosis. Lancet 2004;364:1789-1799.
77. Guo SW, Zheng Y, Lu Y, Liu X, Geng JG. Slit2 overexpression results in increased microvessel density and lesion size in mice with induced endometriosis. Reprod Sci 2013;20:285-298.
78. Hansen-Algenstaedt N, Algenstaedt P, Schaefer C, Hamann A,Wolfram L, Cingöz G, Kilic N, Schwarzloh B, Schroeder M, Joscheck C et al. Neural driven angiogenesis by overexpression of nerve growth factor. Histochem Cell Biol 2006;125: 637-649.
79. Harrison S, Geppetti P. Substance p. Int J Biochem Cell Biol 2001;33:555-576.
80. Herington JL, Bruner-Tran KL, Lucas JA, Osteen KG. Immune interactions in endometriosis. Expert Rev Clin Immunol 2011;7:611-626.
81. Hollman MW, Durieux ME. Local anesthetics and the inflammatory response. Anesthesiology 2000;93:858-875.
82. HonmaY, Araki T, Gianino S, Bruce A, Heuckeroth R, Johnson E, Milbrandt J. Artemin is a vascular-derived neurotropic factor for developing sympathetic neurons. Neuron 2002;35:267-282.
83. Horigome K, Bullock ED, Johnson EM Jr. Effects of nerve growth factor on rat peritoneal mast cells. Survival promotion and immediate-early gene induction. J Biol Chem 1994; 269:2695-2702.
84. Huang EJ, Reichardt LF. Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 2001;24:677-736.
85. Huber AB, Kolodkin AL, Ginty DD, Cloutier JF. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 2003;26:509-563.
86. Indraccolo U, Barbieri F. Effect of palmitoylethanolamide-polydatin combination on chronic pelvic pain associated with endometriosis: preliminary observations. Eur J Obstet Gynecol Reprod Biol 2010;150:76-79.
87. Jones KR, Farinãs I, Backus C, Reichardt LF. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 1994;76:989-999.
88. Kajitani T, Maruyama T, Asada H, Uchida H, Oda H, Uchida S, Miyazaki K, Arase T, Ono M, Yoshimura Y. Possible involvement of nerve growth factor in dysmenorrhea and dyspareunia associated with endometriosis. Endocr J 2013; 60:1155-1164.
89. Kao LC, Germeyer A, Tulac S, Lobo S, Yang JP, Taylor RN, Osteen K, Lessey BA, Giudice LC. Expression profiling of endometrium from women with endometriosis reveals candidate genes for disease-based implantation failure and infertility. Endocrinology 2003;144:2870-2881.
90. Kariagina A, Romanenko D, Ren SG, Chesnokova V. Hypothalamic-pituitary cytokine network. Endocrinology 2004;145:104-112.
91. Kawamoto K, Aoki J, Tanaka A, Itakura A, Hosono H, Arai H, Kiso Y, Matsuda H. Nerve growth factor activates mast cells through the collaborative interaction with lysophosphatidylserine expressed on the membrane surface of activated platelets. J Immunol 2002;168:6412-6419.
92. Kelm Junior AR, Lancellotti CL, Donadio N, Auge AP, Lima SM, Aoki T, Ribeiro PA. Nerve fibers in uterosacral ligaments of women with deep infiltrating endometriosis. J Reprod Immunol 2008;79:93-99.
93. Klagsbrun M, Eichmann A. A role for axon guidance receptors and ligands in blood vessel development and tumor angiogenesis. Cytokine Growth Factor Rev 2005; 16:535-548.
94. Koerber HR, McIlwrath SL, Lawson JJ, Malin SA, Anderson CE, Jankowski MP, Davis BM. Cutaneous C-polymodal fibers lacking TRPV1 are sensitized to heat following inflammation, but fail to drive heat hyperalgesia in the absence of TPV1 containing C-heat fibers. Mol Pain 2010;6:58.
95. Krizsan-Agbas D, Pedchenko T, HasanW, Smith PG. Oestrogen regulates sympathetic neurite outgrowth by modulating brain derived neurotrophic factor synthesis and release by the rodent uterus. Eur J Neurosci 2003;18:2760-2768.
96. Krum JM, Mani N, Rosenstein JM. Angiogenic and astroglial responses to vascular endothelial growth factor administration in adult rat brain. Neuroscience 2002; 110:589-604.
97. Kuruvilla R,Zweifel LS, Glebova NO,Lonze BE,Valdez G,Ye H, Ginty DD.A neurotrophin signalling cascade coordinates sympathetic neuron development through differential control of TrkA trafficking and retrograde signalling. Cell 2004;118:243-255.
98. Lane NE, Schnitzer TJ, Birbara CA, Mokhtarani M, Shelton DL, Smith MD, Brown MT. Tanezumab for the treatment of pain from osteoarthritis of the knee. N Engl J Med 2010;363:1521-1531.
99. Larriveé B, Freitas C, Suchting S, Brunet I, Eichmann A. Guidance of vascular development: lessons from the nervous system. Circ Res 2009;104:428-441.
100. Laschke MW, Menger MD. Anti-angiogenic treatment strategies for the therapy of endometriosis. Hum Reprod Update 2012;18:682-702.
101. Laschke MW, Giebels C, Menger MD. Vasculogenesis: a new piece of the endometriosis puzzle. Hum Reprod Update 2011;17:628-636.
102. Lazarovici P, Marcinkiewicz C, Lelkes PI. Cross talk between the cardiovascular and nervous systems: neurotrophic effects of vascular endothelial growth factor (VEGF) and angiogenic effects of nerve growth factor (NGF)-implications in drug development. Curr Pharm Des 2006;12:2609-2622.
103. le Noble F, Klein C, Tintu A, Pries A, Buschmann I. Neural guidance molecules, tip cells, and mechanical factors in vascular development. Cardiovasc Res 2008; 78:232-241.
104. Leslie C,Ma T, McElhinney B, Leake R, Stewart CJ. Is the detection of endometrial nerve fibers useful in the diagnosis of endometriosis? Int J Gynecol Pathol 2013;32:149-155.
105. Leyendecker G, Kunz G, Noe M, Herbertz M, Mall G. Endometriosis: a dysfunction and disease of the archimetra. Hum Reprod Update 1998;4:752-762.
106. Liu B, Lu KY. Neural invasion in pancreatic carcinoma. Hepatobiliary Pancreat Dis Int 2002;1:469-476.
107. Liu J, Liu X, Duan K, Zhang Y, Guo SW. The expression and functionality of transient receptor potential vanilloid 1 in ovarian endometriomas. Reprod Sci 2012;19:1110-1124.
108. Loeser JD, Treede RD. The Kyoto protocol of IASP Basic Pain Terminology. Pain 2008; 137:473-477.
109. Long H, Sabatier C, Ma L, Plump A, Yuan W, Ornitz DM, Tamada A, Murakami F, Goodman CS, Long JB et al. VEGF-A and Semaphorin3A: modulators of vascular sympathetic innervation. Dev Biol 2009;334:119-132.
110. Lorton D, Lubahn C, Lindquist CA, Schaller J, Washington C, Bellinger DL. Changes in the density and distribution of sympathetic nerves in spleens from Lewis rats with adjuvant-induced arthritis suggest that an injury and sprouting response occurs. J Comp Neurol 2005;489:260-273.
111. Lovell MA, Xie C, Xiong S, Markesbery WR. Wilms' tumor suppressor (WT1) is a mediator of neuronal degeneration associated with the pathogenesis of Alzheimer's disease. Brain Res 2003;983:84-96.
112. Mackenzie F, Ruhrberg C. Diverse roles for VEGF-A in the nervous system. Development 2012;139:1371-1380.
113. Malykhina AP. Neural mechanisms of pelvic organ cross-sensitization. Neuroscience 2007;149:660-672.
114. Mani N, Khaibullina A, Krum JM, Rosenstein JM. Astrocyte growth effects of vascular endothelial growth factor (VEGF) application to perinatal neocortical explants: receptor mediation and signal transduction pathways. Exp Neurol 2005; 192:394-406.
115. Marko SB, Damon DH. VEGF promotes vascular sympathetic innervation. Am J Physiol Heart Circ Physiol 2008;294:H2646-H2652.
116. Marzioni D, Tamagnone L, Capparuccia L, Marchini C, Amici A, Todros T, Bischof P, Neidhart S, Grenningloh G, Castellucci M. Restricted innervation of uterus and placenta during pregnancy: evidence for a role of the repelling signal Semaphorin 3A. Dev Dyn 2004;231:839-848.
117. May K, Becker CM. Endometriosis and angiogenesis. Minerva Ginecol 2008; 60:245-254.
118. May KE, Conduit-Hulbert SA, Villar J, Kirtley S, Kennedy SH, Becker CM. Peripheral biomarkers of endometriosis: a systematic review. Hum Reprod Update 2010; 16:651-674.
119. May KE, Villar J, Kirtley S, Kennedy SH, Becker CM. Endometrial alterations in endometriosis: a systematic review of putative biomarkers. Hum Reprod Update 2011;17:637-653.
120. McAllister SL, McGinty KA, Resuehr D, Berkley KJ. Endometriosis-induced vaginal hyperalgesia in the rat: role of the ectopic growths and their innervation. Pain 2009;147:255-264.
121. McKinnon B, Bersinger NA, Wotzkow C, Mueller MD. Endometriosis-associated nerve fibers, peritoneal fluid cytokine concentrations, and pain in endometriotic lesions from different locations. Fertil Steril 2012;97:373-380.
122. McLaren J, Prentice A, Charnock-Jones DS, Millican SA, Müller KH, Sharkey AM, Smith SK. Vascular endothelial growth factor is produced by peritoneal fluid macrophages in endometriosis and is regulated by ovarian steroids. J Clin Invest 1996;98:482-489.
123. Mechsner S, Schwarz J, Thode J, Loddenkemper C, Salomon DS, Ebert AD. Growth-associated Gap 43 positive sensory nerve fibers accompanied by immature vessels are located in or near peritoneal endometriotic lesions. Fertil Steril 2007;88:583-587.
124. Mechsner S, Kaiser A, Kopf A, Gericke C, Ebert A, Bartley J. A pilot study to evaluate the clinical relevance of endometriosis-associated nerve fibers in peritoneal endometriotic lesions. Fertil Steril 2009;92:1856-1861.
125. Melani M, Weinstein BM. Common factors regulating patterning of the nervous and vascular systems. Annu Rev Cell Dev Biol 2010;26:639-665.
126. Merskey H, Bogduk N. Classification of Chronic Pain, 2nd edn. Seattle, USA: IASP Press, 1994.
127. Miller LE, Weidler C, Falk W, Angele P, Schaumburger J, Schölmerich J, Straub RH. Increased prevalence of semaphorin 3C, a repellent of sympathetic nerve fibers, in the synovial tissue of patients with rheumatoid arthritis. Arthritis Rheum 2004; 50:1156-1163.
128. Morrison TC, Dmitrieva N, Winnard KP, Berkley KJ. Opposing viscerovisceral effects of surgically induced endometriosis and a control abdominal surgery on the rat bladder. Fertil Steril 2006;86:1067-1073.
129. Mortimer D, Fothergill T, Pujic Z, Richards LJ, Goodhill GJ. Growth cone chemotaxis. Trends Neurosci 2008;31:90-98.
130. Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 2002;109:693-705.
131. Nance DM, Sanders VM. Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav Immun 2007;21:736-745.
132. Nap AW, Griffioen AW, Dunselman GA, Bouma-Ter Steege JC, Thijssen VL, Evers JL, Groothuis PG. Antiangiogenesis therapy for endometriosis. J Clin Endocrinol Metab 2004;89:1089-1095.
133. Naska S, Lin DC, Miller FD, Kaplan DR. p75NTR is an obligate signaling receptor required for cues that cause sympathetic neuron growth cone collapse. Mol Cell Neurosci 2010;45:108-120.
134. Newman TA, Bailey JL, Stocker LJ,Woo YL, Macklon NS, Cheong YC. Expression of neuronal markers in the endometrium of women with and those without endometriosis. Hum Reprod 2013;28:2502-2510.
135. Nico B, Mangieri D, Benagiano V, Crivellato E, Ribatti D. Nerve growth factor as an angiogenic factor. Microvasc Res 2008;75:135-141.
136. Nie J, Liu X, Guo SW. Immunoreactivity of oxytocin receptor and transient receptor potential vanilloid type 1 and its correlation with dysmenorrhea in adenomyosis. Am J Obstet Gynecol 2010;202:346.e1-8.
137. Nie J, Liu X, Zheng Y, Geng JG, Guo SW. Increased immunoreactivity to SLIT/ROBO1 and its correlation with severity of dysmenorrhea in adenomyosis. Fertil Steril 2011; 95:1164-1167.
138. Novella-Maestre E, Herraiz S, Vila-Vives JM, Carda C, Ruiz-Sauri A, Pellicer A. Effect of antiangiogenic treatment on peritoneal endometriosis-associated nerve fibers. Fertil Steril 2012;98:1209-1217.
139. Odagiri K, Konno R, FujiwaraH, Netsu S, Yang C, Suzuki M. Smooth muscle metaplasia and innervation in interstitium of endometriotic lesions related to pain. Fertil Steril 2009;92:1525-1531.
140. O'Sullivan M, Clayton N, Breslin NP, Harman I, Bountra C, McLaren A, O'Morain CA. Increased mast cells in the irritable bowel syndrome. Neurogastroenterol Motil 2000; 12:449-457.
141. Pezzone MA, Liang R, Fraser MO. A model of neural cross-talk and irritation in the pelvis: implications for the overlap of chronic pelvic pain disorders. Gastroenterology 2005;128:1953-1964.
142. Poli-Neto OB, Filho AA, Rosa e Silva JC, Barbosa Hde F, Candido Dos Reis FJ, Nogueira AA. Increased capsaicin receptor TRPV1 in the peritoneum of women with chronic pelvic pain. Clin J Pain 2009;25:218-222.
143. Pongratz G, Straub RH. Role of peripheral nerve fibres in acute and chronic inflammation in arthritis. Nat Rev Rheumatol 2013;9:117-126.
144. Proctor ML, Latthe PM, Farquhar CM, Khan KS, Johnson NP. Surgical interruption of pelvic nerve pathways for primary and secondary dysmenorrhoea. Cochrane Database Syst Rev 2005;4:CD001896.
145. Quinn M. Uterine innervation in adenomyosis. J Obstet Gynaecol 2007;27:287-291.
146. Quinn MJ, Armstrong G. Uterine nerve fibre proliferation in advanced endometriosis. J Obstet Gynaecol 2004;24:932-933.
147. Quinn MJ, Kirk N. Uterosacral reinnervation in parous endometriosis. J Obstet Gynaecol 2004;24:189-190.
148. Raddant AC, Russo AF. Calcitonin gene-related peptide in migraine: intersection of peripheral inflammation and central modulation. Expert Rev Mol Med 2011;13:e36.
149. Raychaudhuri SK, Raychaudhuri SP, Weltman H, Farber EM. Effect of nerve growth factor on endothelial cell biology: proliferation and adherence molecule expression on human dermal microvascular endothelial cells. Arch Dermatol Res 2001;293:291-295.
150. Ren K, Ruda MA, Jacobowitz DM. Immunohistochemical localization of calretinin in the dorsal root ganglion and spinal cord of the rat. Brain Res Bull 1993;31:13-22.
151. Richeri A, Bianchimano P, Mármol NM, Viettro L, Cowen T, Brauer MM. Plasticity in rat uterine sympathetic nerves: the role of TrkA and p75 nerve growth factor receptors. J Anat 2005;207:125-134.
152. Richeri A, Chalar C, Martínez G, Greif G, Bianchimano P, Brauer MM. Estrogen up-regulation of semaphorin 3F correlates with sympathetic denervation of the rat uterus. Auton Neurosci 2011;164:43-50.
153. Rocha MG, e Silva JC, Ribeiro da Silva A, Candido Dos Reis FJ, Nogueira AA, Poli-Neto OB. TRPV1 expression on peritoneal endometriosis foci is associated with chronic pelvic pain. Reprod Sci 2011;18:511-515.
154. Ruiz de Almodovar C, Fabre PJ, Knevels E, Coulon C, Segura I, Haddick PC, Aerts L, Delattin N, Strasser G, Oh WJ et al. VEGF mediates commissural axon chemoattraction through its receptor Flk1. Neuron 2011;70:966-978.
155. Sacco K, Portelli M, Pollacco J, Schembri-Wismayer P, Calleja-Agius J. The role of prostaglandin E2 in endometriosis. Gynecol Endocrinol 2012;28:134-138.
156. Samah B, Porcheray F, Gras G. Neurotrophins modulate monocyte chemotaxis without affecting macrophage function. Clin Exp Immunol 2008;151:476-486.
157. Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol 1927;3:93-110.
158. Sant GR, Kempuraj D, Marchand JE, Theoharides TC. The mast cell in interstitial cystitis: role in pathophysiology and pathogenesis. Urology 2007;69:34-40.
159. Sekiguchi H, Ii M, Jujo K, Thorne T, Ito A, Klyachko E, Hamada H, Kessler JA, Tabata Y, Kawana M et al. Estradiol promotes neural stem cell differentiation into endothelial lineage and angiogenesis in injured peripheral nerve. Angiogenesis 2013; 16:45-58.
160. Shen F, Liu X, Geng JG, Guo SW. Increased immunoreactivity to SLIT/ROBO1 in ovarian endometriomas: a likely constituent biomarker for recurrence. Am J Pathol 2009;175:479-488.
161. Signorile PG, Campioni M, Vincenzi B, D'Avino A, Baldi A. Rectovaginal septum endometriosis: an immunohistochemical analysis of 62 cases. In Vivo 2009; 23:459-464.
162. Silveira CG, Finas D, Hunold P, Kö ster F, Stroschein K, Canny GO, Moldenhauer G, Altevogt P, Rody A, Hornung D. L1 cell adhesion molecule as a potential therapeutic target in murine models of endometriosis using a monoclonal antibody approach. PLoS One 2013;8:e82512.
163. Skaper SD. The biology of neurotrophins, signalling pathways, and functional peptide mimetics of neurotrophins and their receptors. CNS Neurol Disord Drug Targets 2008;7:46-62.
164. Snider WD, McMahon SB. Tackling pain at the source: new ideas about nociceptors. Neuron 1998;20:629-632.
165. Soares SR, Martínez-Varea A, Hidalgo-Mora JJ, Pellicer A. Pharmacologic therapies in endometriosis: a systematic review. Fertil Steril 2012;98:529-555.
166. Steinle JJ, Granger HJ. Nerve growth factor regulates human choroidal, but not retinal, endothelial cell migration and proliferation. Auton Neurosci 2003;108:57-62.
167. Stratton P, Berkley KJ. Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications. Hum Reprod Update 2011;17:327-346.
168. Straub RH. Autoimmune disease and innervation. Brain Behav Immun 2007; 21:528-534.
169. StraubRH, Mayer M, Kreutz M, Leeb S, Schölmerich J, FalkW. Neurotransmitters of the sympathetic nerve terminal are powerful chemoattractants for monocytes. J Leukoc Biol 2000;67:553-558.
170. Tamburro S, Canis M, Albuisson E, Dechelotte P, Darcha C, Mage G. Expression of transforming growth factor beta1 in nerve fibers is related to dysmenorrhea and laparoscopic appearance of endometriotic implants. Fertil Steril 2003; 80:1131-1136.
171. Taylor DC, Pierau FK, Schmid H. The use of fluorescent tracers in the peripheral sensory nervous system. J Neurosci Methods 1983;8:211-224.
172. Taylor RN, Yu J, Torres PB, SchickedanzAC, Park JK, Mueller MD,Sidell N. Mechanistic and therapeutic implications of angiogenesis in endometriosis. Reprod Sci 2009; 16:140-146.
173. Tokushige N, Markham R, Russell P, Fraser IS. Nervefibres in peritoneal endometriosis. Hum Reprod 2006a;21:3001-3007.
174. Tokushige N, Markham R, Russell P, Fraser IS. High density of small nerve fibres in the functional layer of the endometrium in women with endometriosis. Hum Reprod 2006b;21:782-787.
175. Tokushige N, Markham R, Russell P, Fraser IS. Different types of small nerve fibers in eutopic endometrium and myometrium in women with endometriosis. Fertil Steril 2007;88:795-803.
176. Tokushige N, Markham R, Russell P, Fraser IS. Effects of hormonal treatment on nerve fibers in endometrium and myometrium in women with endometriosis. Fertil Steril 2008;90:1589-1598.
177. Tokushige N, Markham R, Russell P, Fraser IS. Effect of progestogens and combined oral contraceptives on nerve fibers in peritoneal endometriosis. Fertil Steril 2009; 92:1234-1239.
178. Tokushige N, Russell P, Black K, BarreraH, Dubinovsky S, Markham R, Fraser IS. Nerve fibers in ovarian endometriomas. Fertil Steril 2010;94:1944-1947.
179. Tran LV, Tokushige N, Berbic M, Markham R, Fraser IS. Macrophages and nerve fibres in peritoneal endometriosis. Hum Reprod 2009;24:835-841.
180. Tulandi T, Felemban A, Chen MF. Nerve fibers and histopathology of endometriosis-harboring peritoneum. J Am Assoc Gynecol Laparosc 2001;8:95-98.
181. TurriniP, Gaetano C, Antonelli A, CapogrossiMC,Aloe L. Nervegrowth factor induces angiogenic activity in a mouse model of hindlimb ischemia. Neurosci Lett 2002; 323:109-112.
182. Ustinova EE, Fraser MO, Pezzone MA. Colonic irritation in the rat sensitizes urinary bladder afferents to mechanical and chemical stimuli: an afferent origin of pelvic organ cross-sensitization. Am J Physiol Renal Physiol 2006;290: F1478-F1487.
183. Ustinova EE, Gutkin DW, Pezzone MA. Sensitization of pelvic nerve afferents and mast cell infiltration in the urinary bladder following chronic colonic irritation is mediated by neuropeptides. Am J Physiol Renal Physiol 2007;292:F123-F130.
184. Ustinova EE, Fraser MO, Pezzone MA. Cross-talk and sensitization of bladder afferent nerves. Neurourol Urodyn 2010;29:77-81.
185. Vercellini P, Fedele L, Aimi G, Pietropaolo G, Consonni D, Crosignani PG. Association between endometriosis stage, lesion type, patient characteristics and severity of pelvic pain symptoms: a multivariate analysis of over 1000 patients. Hum Reprod 2007;22:266-271.
186. Vigé X, Costa E, Wise BC. Mechanism of nerve growth factor mRNA regulation by interleukin-1 and basic fibroblast growth factor in primary cultures of rat astrocytes. Mol Pharmacol 1991;40:186-192.
187. Wagner KD,Wagner N, Vidal VP, SchleyG, Wilhelm D, Schedl A, Englert C, Scholz H. The Wilms' tumor gene Wt1 is required for normal development of the retina. EMBO J 2002;21:1398-1405.
188. Wagner N,Wagner KD, Hammes A, Kirschner KM, Vidal VP, Schedl A, Scholz H. A splice variant of the Wilms' tumour suppressor Wt1 is required for normal development of the olfactory system. Development 2005;132:1327-1336.
189. Wang L, Zeng H,Wang P, Soker S, MukhopadhyayD. Neuropilin-1-mediated vascular permeability factor/vascular endothelial growth factor-dependent endothelial cell migration. J Biol Chem 2003;278:48848-48860.
190. Wang L, Dutta SK, Kojima T, Xu X, Khosravi-Far R, Ekker SC, Mukhopadhyay D. Neuropilin-1 modulates p53/caspases axis to promote endothelial cell survival. PLoS One 2007;2:e1161.
191. Wang G, Tokushige N, Russell P, Dubinovsky S, Markham R, Fraser IS. Hyperinnervation in intestinal deep infiltrating endometriosis. J Minim Invasive Gynecol 2009a;16:713-719.
192. Wang G, Tokushige N, Markham R, Fraser IS. Rich innervation of deep infiltrating endometriosis. Hum Reprod 2009b;24:827-834.
193. Wang G, Tokushige N, Fraser IS. Nerve fibers and menstrual cycle in peritoneal endometriosis. Fertil Steril 2011;95:2772-2774.
194. Weidler C, Holzer C, Harbuz M, Hofbauer R, Angele P, Schölmerich J, Straub RH. Low density of sympathetic nerve fibres and increased density of brain derived neurotrophic factor positive cells in RA synovium. Ann Rheum Dis 2005; 64:13-20.
195. Wickström K, Bruse C, Sjösten A, Spira J, Edelstam G. Pertubation with lignocaine as a new treatment of dysmenorrhea due to endometriosis: a randomized controlled trial. Hum Reprod 2012;27:695-701.
196. Winnard KP, Dmitrieva N, Berkley KJ. Cross-organ interactions between reproductive, gastrointestinal, and urinary tracts: modulation by estrous stage and involvement of the hypogastric nerve. Am J Physiol Regul Integr Comp Physiol 2006;291: R1592-R1601.
197. Yang H, Kim TH, Lee HH, Choi KC, Hong YP, Leung PC, Jeung EB. Expression of calbindin-D28k and its regulation by estrogen in the human endometrium during the menstrual cycle. Reprod Biol Endocrinol 2011;9:28.
198. Young VJ, Brown JK, Saunders PT, Horne AW. The role of the peritoneum in the pathogenesis of endometriosis. Hum Reprod Update 2013;19:558-569.
199. Zhang G, Dmitrieva N, Liu Y, McGinty KA, Berkley KJ. Endometriosis as a neurovascular condition: estrous variations in innervation, vascularization, and growth factor content of ectopic endometrial cysts in the rat. Am J Physiol Regul Integr Comp Physiol 2008;294:R162-R171.
200. Zhang X, Lu B, Huang X, Xu H, Zhou C, Lin J. Endometrial nerve fibers in women with endometriosis, adenomyosis, and uterine fibroids. Fertil Steril 2009;92:1799-1801.
201. Zhang X, Lu B, Huang X, Xu H, Zhou C, Lin J. Innervation of endometrium and myometrium in women with painful adenomyosis and uterine fibroids. Fertil Steril 2010a;94:730-737.
202. Zhang X, Yao H, Huang X, Lu B, Xu H, Zhou C. Nerve fibres in ovarian endometriotic lesions in women with ovarian endometriosis. Hum Reprod 2010b; 25:392-397.
203. Zhang F, Yang Y,Wang Y. Association between TGF- β1-509C/T polymorphism and endometriosis: a systematic review and meta-analysis. Eur J Obstet Gynecol Reprod Biol 2012;164:121-126.
204. Zheng Y, Liu X, Guo SW. Therapeutic potential of andrographolide for treating endometriosis. Hum Reprod 2012;27:1300-1313.
205. Zoubina EV, Mize AL, Alper RH, Smith PG. Acute and chronic estrogen supplementation decreases uterine sympathetic innervation in ovariectomized adult virgin rats. Histol Histopathol 2001;16:989-996.